Skip to main content
Log in

Differential response of the epidermal growth factor receptor tyrosine kinase activity to several plant and mammalian lectins

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Biosignalling via lectins may involve modulation of protein kinase activities. This aspect of the biological action of mammalian and plant lectins has been investigated for their effect on the activity of the isolated epidermal growth factor receptor (EGFR). The constitutive tyrosine kinase activity of the epidermal growth factor receptor from rat liver, isolated by calmodulin-affinity chromatography, was activated by concanavalin A (ConA), and wheat germ agglutinin (WGA) to a similar extent as the measured enhancement induced by EGF. In contrast, two mannose-specific lectins, the mannan-binding protein (MBP) and serum amyloid P component (SAP), isolated from human serum, have inhibitory effects, both in the absence and presence of EGF. The differential effects of these lectins were tested using as phosphorylatable substrates a co-polymer of glutamic acid-tyrosine, as well as calmodulin. However, two galactoside-specific lectins, the laminin-binding β-galactoside-binding 14 kDa lectin, isolated from bovine heart (14K-BHL), and the α/β-galactoside-binding lectin, isolated from mistletoe (Viscum album L.) leaves (VAA), do not inhibit the EGFR tyrosine kinase activity. The sugar dependence of the lectin-mediated action was studied by inhibition assays. Mannose and a mannose-containing neoglycoprotein prevent the activating effect of ConA, and N-acetyl-D-glucosamine partially prevents the activation produced by WGA. However, mannose and mannose-containing neoglycoprotein were ineffective to reduce the inhibitory effect of MBP or SAP. Although the response to binding of ConA and WGA was different to that of MBP or SAP with respect to the tyrosine kinase activity of the EGFR, it should be noted that the four lectins inhibited the binding of [125I]EGF to its receptor with similar efficiency.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

EGF:

epidermal growth factor

EGFR:

epidermal growth factor receptor

ConA:

concanavalin A

MBP:

mannan-binding protein

SAP:

serum amyloid P component

WGA:

wheat germ agglutinin

14K-BHL:

bovine heart 14 kDa lectin

VAA:

Viscum album L. (mistletoe) agglutinin

EGTA:

[ethylenebis(oxyethylenenitrilo)]-tetraacetic acid; poly(Glu:Tyr)-co-polymer of L-glutamic acid and L-tyrosine

Hepes:

4-(2-hydroxyethyl)-1-piperazinethanesulfonic acid

Tris:

tris(hydroxymethyl)-aminomethane

DSS:

suberic acid bis(N-hydroxy-succinimide ester)

PMSF:

phenylmethanesulfonyl fluoride

Man:

mannose

Gal:

galactose

BSA:

bovine serum albumin

Man-BSA:

neoglycoprotein containing α-D-mannose

Lac-BSA:

neoglycoprotein containing β-lactose

Gal-BSA:

neoglycoprotein containing galactose

References

  1. Blithe DL: Biological functions of oligosaccharides on glycoproteins. Trends Glycosci. Glycotechnol 5: 81–98, 1993

    Google Scholar 

  2. Lis H, Sharon N; Protein glycosylation. Structure and functional aspects. Eur J Biochem 218: 1–27, 1993

    PubMed  Google Scholar 

  3. Varki A: Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3: 97–130, 1993

    PubMed  Google Scholar 

  4. Sairam MR: Role of carbohydrates in glycoprotein hormone signal transduction. FASEB J 3: 1915–1926, 1989

    PubMed  Google Scholar 

  5. Santer R, Leung YK, Alliet P, Lebenthal E, Leung PC: The role of carbohydrate moieties of cholecystokinin receptor in cholecystokinin octapeptide binding: alteration of binding data by specific lectins. Biochim Biophys Acta 1051: 78–83, 1990

    PubMed  Google Scholar 

  6. Leconte I, Auzan C, Debant A, Clauser E: N-linked oligosaccharide chains of the insulin receptor β-subunit are essential for transmembrane signalling. J Biol Chem 267: 17415–17423, 1992

    PubMed  Google Scholar 

  7. Morie H, Watanabe Y: A possible role of carbohydrate moieties in prostaglandin D2 and prostaglandin E2 receptor proteins from the porcine temporal cortex. Arch Biochem Biophys 292: 121–127, 1992

    PubMed  Google Scholar 

  8. Gabius HJ: Detection and functions of mammalian lectins-with emphasis on membrane lectins. Biochim Biophys Acta 1071: 1–18, 1991

    PubMed  Google Scholar 

  9. Scudder P, Childs RA, Feizi T, Joziasse DH, Schiphorst WECM, van den Eijnden DH: Bovine heart lectin stimulates β-D-galactoside α-2,6-sialytransferase of bovine colostrum. Biochem Biophys Res Commun 104: 272–278, 1992

    Google Scholar 

  10. Carpenter G: Receptors for epidermal growth factor and other polypeptide mitogens. Annu Rev Biochem 56: 881–914, 1987

    PubMed  Google Scholar 

  11. Ullrich A, Schlessinger J: Signal transduction by receptors with tyrosine kinase activity. Cell 61: 203–212, 1990

    PubMed  Google Scholar 

  12. Hernández-Sotomayor SMT, Carpenter G: Epidermal growth factor receptor: Elements of intracellular communication. J Memb Biol 128: 81–89, 1992

    Google Scholar 

  13. Ullrich A, Coussens L, Hayflick JS, Dull TJ, Gray A, Tam AW, Lee J, Yarden Y, Libermann TA, Schlessinger J, Downward J, Mayes ELV, Whittle N, Waterfield MD, Seeburg PH: Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309: 418–425, 1984

    PubMed  Google Scholar 

  14. Bertics PJ, Gill GN: Self-phosphorylation enhances the protein-tyrosine kinase activity of the epidermal growth factor receptor. J Biol Chem 260: 14642–14647, 1985

    PubMed  Google Scholar 

  15. Margolis BL, Lax I, Kris R, Dombalagian M, Honegger AM, Howk R, Givol D, Ullrich A, Schlessinger J: All autophosphorylation sites of epidermal growth factor (EGF) receptor and HER2/neu are located in their carboxyl-terminal tails. Identification of a novel site in EGF receptor. J Biol Chem 264: 10667–10671, 1989

    PubMed  Google Scholar 

  16. Decker SJ: Transmembrane signaling by epidermal growth factor receptors lacking autophosphorylation sites. J Biol Chem 268: 9176–9179, 1993

    PubMed  Google Scholar 

  17. Soderquist AM, Carpenter G: Glycosylation of the epidermal growth factor receptor in A-431 cells. The contribution of carbohydrate to receptor function. J Biol Chem 259: 12586–12594, 1984

    PubMed  Google Scholar 

  18. Carpenter G, Cohen S: Influence of lectins on the binding of125I-labeled EGF to human fibroblasts. Biochem Biophys Res Commun 79: 545–552, 1977

    PubMed  Google Scholar 

  19. Ballmer K, Burger MM: Modulation of EGF binding and action by succinylated concanavalin A in fibroblast cell cultures. J Supramol Struct 14: 209–214, 1980

    PubMed  Google Scholar 

  20. Vale RD, Shooter EM: Epidermal growth factor receptors on PC12 cells: Alterations of binding properties by lectins. J Cell Biochem 22: 99–109, 1983

    PubMed  Google Scholar 

  21. Boonstra J, Mummery CL, Van der Saag PT, De Laat SW: Two receptor classes for epidermal grwoth factor on pheochromocytoma cells, distinguishable by temperature, lectins, and tumor promoter. J Cell Physiol 123: 347–352, 1985

    PubMed  Google Scholar 

  22. Childs RA, Gregorion M, Scudder P, Thorpe SJ, Rees AR, Feizi T: Blood group-active carbohydrate chains on the receptor for epidermal growth factor of A431 cells. EMBO J 3: 2227–2233, 1984

    PubMed  Google Scholar 

  23. Todderud G, Carpenter G: Presence of mannose phosphate on the epidermal growth factor receptor in A-431 cells. J Biol Chem 263: 17893–17896, 1988

    PubMed  Google Scholar 

  24. Soderquist AM, Stoscheck C, Carpenter G: Similarities in glycosylation and transport between the secreted and plasma membrane forms of the epidermal growth factor receptor in A-431 cells. J Cell Physiol 136: 447–454, 1988

    PubMed  Google Scholar 

  25. Feizi T, Childs RA: Carbohydrate structures of glycoproteins and glycolipids as differentiation antigens, tumor-associated antigens and components of receptor systems. Trends Biochem Sci 10: 24–29, 1985

    Google Scholar 

  26. Kaplowitz PB, Haar JL: Antimitogenic actions of lectins in cultured human fibroblasts. J Cell Physiol 136: 13–22, 1988

    PubMed  Google Scholar 

  27. Moseley JM, Suva LJ: Molecular characterization of the EGF receptor and involvement of glycosyl moieties in the binding of EGF to its receptor on a clonal osteosarcoma cell line, UMR 106-06. Calcif Tissue Int 38: 109–114, 1986

    PubMed  Google Scholar 

  28. Rozengurt E: Early signals in the mitogenic response. Science 234: 161–166, 1986

    PubMed  Google Scholar 

  29. Moolenaar WH, Aerts RJ, Tertoolen LGJ, De Laat SW: The epidermal growth factor-induced calcium signal in A431 cells. J Biol Chem 261: 279–284 1986

    PubMed  Google Scholar 

  30. Pandiella A, Beguinot L, Velu TJ, Meldolesi J: Transmembrane signalling at epidermal growth factor receptors overexpressed in NIH 3T3 cells. Phosphoinositide hydrolysis, cytosolic Ca2+ increase and alkalinization correlate with epidermal-growth-factor-induced cell proliferation. Biochem J 254: 223–228 1988

    PubMed  Google Scholar 

  31. Pandiella A, Beguinot L, Vicentini LM, Meldolesi J: Transmembrane signalling at the epidermal growth factor receptor. Trends Pharm Sci 10: 411–414 1989

    PubMed  Google Scholar 

  32. Cheyette TE, Gross DJ: Epidermal growth factor-stimulated calcium ion transients in individual A431 cells: initiation kinetics and ligand concentration dependence. Cell Regul 2: 827–840 1991

    PubMed  Google Scholar 

  33. Wheeler LA, Sachs G, De Vries G, Goodrum D, Woldemussie E, Muallem S: Manoalide, a natural sesterterpenoid that inhibits calcium channels. J Biol Chem 262: 6531–6538 1987

    PubMed  Google Scholar 

  34. Green J, Muallem S: A common mechanism for activation of the Na+/H+ exchanger by different types of stimuli. FASEB J 3: 2408–2414, 1989

    PubMed  Google Scholar 

  35. Kubak BM, Potempa LA, Anderson B, Mahklouf S, Venegas M, Gewurz H, Gewurz AT: Evidence that serum amyloid P component binds to mannose-terminated sequences of polysaccharides and glycoproteins. Mol Immunol 25: 851–858

  36. Loveless RW, Floyd-O'Sullivan G, Raynes JG, Yuen C-T, Feizi T: Human serum amyloid P is a multispecific adhesive protein whose ligands include 6-phosphorylated mannose and the 3-sulfated saccharides galactose, N-acetylgalactosamine and glucuronic acid. EMBO J 11: 813–819, 1992

    PubMed  Google Scholar 

  37. Reid KBM: Structure/function relationships in the collectins (mammalian lectins containing collagen-like regions). Biochem Soc Trans 21: 464–468, 1993

    PubMed  Google Scholar 

  38. San José E, Benguría A, Geller P, Villalobo A: Calmodulin inhibits the epidermal growth factor receptor tyrosine kinase. J Biol Chem 267: 15237–15245, 1992

    PubMed  Google Scholar 

  39. Benguría A, Hernández-Perera O, Martínez-Pastor MT, Sacks DB, Villalobo A: Phosphorylation of calmodulin by the epidermal-growth-factor-receptor tyrosine kinase. Eur J Biochem 224: 909–916, 1994

    PubMed  Google Scholar 

  40. Brown AE, Lok MP, Elovson J: Improved method for the isolation of rat liver plasma membrane. Biochim Biophys Acta 426: 418–432, 1976

    PubMed  Google Scholar 

  41. Church JG, Ghosh S, Roufogalis BD, Villalobo A: Endogenous hyperphosphorylation in plasma membrane from an ascites hepatocarcinoma cell line. Biochem Cell Biol 66: 1–12, 1988

    PubMed  Google Scholar 

  42. San José E, Benguría A, Gabius JH, Villalobo A: Effects of lectins on adenylylation and phosphorylation of plasma membrane proteins. In: H.-J. Gabius and S. Gabius (eds). Lectins and Glycobiology. Springer Verlag, Heidelberg/New York, 1993, pp 329–355

    Google Scholar 

  43. Gabious HJ, Gabius S (eds): Lectins and Glycobiology. Springer Publication Company, Heidelberg/New York, 1993

    Google Scholar 

  44. Gabious HJ: Influence of type of linkage and spacer on the interaction of β-galactoside-binding proteins with immobilized affinity ligands. Anal Biochem 189: 91–94, 1990

    PubMed  Google Scholar 

  45. Kyogashima M, Krivan HC, Schweinle JE, Ginsburg V, Holt GD: Glycosphingolipid-binding specificity of the mannose-binding protein human sera. Arch Biochem Biophys 283: 217–222, 1990

    PubMed  Google Scholar 

  46. De Beer FC, Pepys MB: Isolation of human C-reactive protein and serum amyloid P component. J Immunol Meth 50: 17–31, 1982

    Google Scholar 

  47. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685, 1970

    PubMed  Google Scholar 

  48. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275, 1951

    PubMed  Google Scholar 

  49. Goldstein D: Calculation of the concentrations of free cations and cation-ligand complexes in solutions containing multiple divalent cations and ligands. Biophys J 26: 235–242, 1979

    PubMed  Google Scholar 

  50. Yarden Y, Schlessinger J: Self-phosphorylation of epidermal growth factor receptor: Evidence for a model of intermolecular allosteric activation. Biochemistry 26: 1434–1442, 1987

    PubMed  Google Scholar 

  51. Ezekowitz RAB, Kuhlman M, Groopman JE, Byrn RA: A human serum mannose-binding protein inhibitsin vitro infection by the human immunodeficiency virus. J Exp Med 169: 185–196, 1989

    PubMed  Google Scholar 

  52. Mann KK, André S, Gabious HJ, Sharp JG: Phenotype associated lectin-binding profile of blood and leukemic cells: a comparative analysis of mannose- and galactose-binding lectins from plants and human serum/placenta. Eur J Cell Biol: (in press), 1994

  53. Hartree AS, Renwick AGC: Molecular structures of glycoprotein hormones and functions of the carbohydrate components. Biochem J 287: 665–679, 1992

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeng, FY., Benguría, A., Kafert, S. et al. Differential response of the epidermal growth factor receptor tyrosine kinase activity to several plant and mammalian lectins. Mol Cell Biochem 142, 117–124 (1995). https://doi.org/10.1007/BF00928932

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00928932

Key Words

Navigation